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15 Genetic and Metabolic Aspects of Primary and Secondary Metabolism of the Zygomycetes

  • Kerstin Voigt
  • Thomas Wolf
  • Katrin Ochsenreiter
  • Gábor Nagy
  • Kerstin Kaerger
  • Ekaterina Shelest
  • Tamás Papp
Chapter
Part of the The Mycota book series (MYCOTA, volume III)

Abstract

Basal lineages of the kingdom of fungi comprise terrestrial and aquatic fungi, which are traditionally summarized as Chytridiomycota and Zygomycota in a colloquial sense. The zygomycetes build up the most basal lineage among the terrestrial fungi. As the earliest fungi to conquer terrestrial habitats, they facilitated early coevolution with other land-dwelling microorganisms with implications on the primary and secondary metabolism which is adaptive to the life in soil. Advances in next-generation genome sequencing allow us to gain a new layer of knowledge with respect to their metabolism and its regulation. Recent revisions of the metabolic potential of zygomycetes using genome mining suggested a hidden potential for the production of secondary metabolites. First insights suggest a revision of our understanding of the importance and mode of action of metabolic pathways revealing a fascinating potential to produce novel natural compounds. The aim of this review is to draw attention to the zygomycetes as a unique fungal group and to inspire the scientific community to explore its potential as participants in complex ecosystems for innovative metabolic regulatory frameworks and novel compounds.

Keywords

Fumaric Acid Carotenoid Biosynthesis Mucor Circinelloides Carotenoid Biosynthesis Gene Rhizopus Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abe A, Oda Y, Asano K, Sone T (2007) Rhizopus delemar is the proper name for Rhizopus oryzae fumaric-malic acid producers. Mycologia 99:714–722PubMedCrossRefGoogle Scholar
  2. Álvarez V, Rodríguez-Sáiz M, de la Fuente JL, Gudiña EJ, Godio RP, Martín JF, Barredo JL (2006) The crtS gene of Xanthophyllomyces dendrorhous encodes a novel cytochrome-P450 hydroxylase involved in the conversion of β-carotene into astaxanthin and other xanthophylls. Fungal Genet Biol 43:261–272PubMedCrossRefGoogle Scholar
  3. Anonymus (2007) Product focus: maleic anhydride. Chem Week 39Google Scholar
  4. Appel KF, Wolff AM, Arnau J (2004) A multicopy vector system for genetic studies in Mucor circinelloides and other zygomycetes. Mol Genet Genomics 271:595–602PubMedCrossRefGoogle Scholar
  5. Arrach N, Fernández-Martín R, Cerdá-Olmedo E, Avalos J (2001) A single gene for lycopene cyclase, phytoene synthase, and regulation of carotene biosynthesis in Phycomyces. Proc Natl Acad Sci USA 98:1687–1692PubMedCentralPubMedCrossRefGoogle Scholar
  6. Azeke MA, Greiner R, Jany KD (2011) Purification and characterization of two intracellular phytases from the tempeh fungus Rhizopus oligosporus. J Food Biochem 35:213–227CrossRefGoogle Scholar
  7. Bai DM, Li SZ, Liu ZL, Cui ZF (2008) Enhanced L-(+)-lactic acid production by an adapted strain of Rhizopus oryzae using corncob hydrolysate. Appl Biochem Biotechnol 144:79–85PubMedCrossRefGoogle Scholar
  8. Bartnicki-Garcia S (1968) Control of dimorphism in Mucor by hexoses: inhibition of hyphal morphogenesis. J Bacteriol 96:1586–1594PubMedCentralPubMedGoogle Scholar
  9. Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326–338PubMedCrossRefGoogle Scholar
  10. Benny GL, Humber RA, Voigt K (2014) Zygomycetous Fungi: phylum Entomophthoromycota and subphyla Kickxellomycotina, Mortierellomycotina, Mucoromycotina, and Zoopagomycotina. In: McLaughlin DJ, Spatafora JW (eds) The Mycota, vol VIIA, 2nd edn, Systematics and evolution. Springer, Berlin, pp 209–250, Chapter 8Google Scholar
  11. Bianciotto V, Lumini E, Bonfante P, Vandamme P (2003) “Candidatus Glomeribacter gigasporarum” gen. nov, sp. nov., an endosymbiont of arbuscular mycorrhizal fungi. Int J Syst Evol Microbiol 53:121–124PubMedCrossRefGoogle Scholar
  12. Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. Biol Lett 7:574–577PubMedCentralPubMedCrossRefGoogle Scholar
  13. Bitar D, Van Cauteren D, Lanternier F, Dannaoui E, Che D, Dromer F, Desenclos JC, Lortholary O (2009) Increasing incidence of zygomycosis (mucormycosis), France, 1997-2006. Emerg Infect Dis 15:1395–1401PubMedCentralPubMedCrossRefGoogle Scholar
  14. Bonito G, Gryganskyi A, Hameed K, Schadt C, Pelletier D, Schaefer A, Tuskan G, Labbe J, Martin F, Doktycz M, LaButti K, Ohm R, Grigoriev I, Vilgalys R (2013) Co-evolution of Mortierella elongata and its endosymbiotic bacterium. In: Abstracts submitted for presentation at the 2013 APS-MSA joint meeting, Austin, TX (2013-08-10–2013-08-14). St. Paul. American Phytopathological Society. Phytopathology 103 (6, Suppl 2):18–19 Presented at APS-MSA Joint MeetingGoogle Scholar
  15. Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32PubMedCrossRefGoogle Scholar
  16. Bulut S, Elibol M, Ozer D (2009) Optimization of process parameters and culture medium for L-(+)-lactic acid production by Rhizopus oryzae. J Chem Eng Jpn 42:589–595CrossRefGoogle Scholar
  17. Burmester A, Richter M, Schultze K, Voelz K, Schachtschabel D, Boland W, Wöstemeyer J, Schimek C (2007) Cleavage of β-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated β-carotene oxygenase. Fungal Genet Biol 44:1096–1108PubMedCrossRefGoogle Scholar
  18. Cao NJ, Du JX, Gong CS, Tsao GT (1996) Simultaneous production and recovery of fumaric acid from immobilized Rhizopus oryzae with a rotary biofilm contractor and adsorption column. Appl Environ Microbiol 62:2926–2931PubMedCentralPubMedGoogle Scholar
  19. Casadevall A, Pirofski L (2001) Host-pathogen interactions. The attributes of virulence. J Infect Dis 184(3):337–344PubMedCrossRefGoogle Scholar
  20. Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? BioSystems 14:461–481PubMedCrossRefGoogle Scholar
  21. Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266PubMedCrossRefGoogle Scholar
  22. Chakrabarti A, Chatterjee SS, Shivaprakash MR (2008) Overview of opportunistic fungal infections in India. Nihon Ishinkin Gakkai Zasshi 49:165–172PubMedCrossRefGoogle Scholar
  23. Chakrabarti A, Chatterjee SS, Das A, Panda N, Shivaprakash MR, Kaur A, Varma SC, Singhi S, Bhansali A, Sakhuja V (2009) Invasive zygomycosis in India: experience in a tertiary care hospital. Postgrad Med J 85:573–581PubMedCrossRefGoogle Scholar
  24. Chamilos G, Lewis RE, Kontoyiannis DP (2007) Multidrug-resistant endosymbiotic bacteria account for the emergence of zygomycosis: a hypothesis. Fungal Genet Biol 44(2):88–92PubMedCrossRefGoogle Scholar
  25. Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C, Clum A, LaButti KM, Lindquist EA, Yee Ngan C, Ohm RA, Salamov AA, Grigoriev IV, Spatafora JW, Berbee ML (2015) Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7(6):1590–1601PubMedCentralPubMedCrossRefGoogle Scholar
  26. Chatzifragkou A, Makri A, Belka A, Bellou S, Mavrou M, Mastoridou M, Mystrioti P, Onjaro G, Aggelis G, Papanikolaou S (2011) Biotechnological conversions of biodiesel derived waste glycerol by yeast and fungal species. Energy 36:1097–1108CrossRefGoogle Scholar
  27. Chaudhuri S, Ghosh S, Bhattacharyya DK, Bandyopadhyay S (1998) Effect of mustard meal on the production of arachidonic acid by Mortierella elongata SC-208. J Am Oil Chem Soc 75:1053–1055Google Scholar
  28. Chayakulkeeree M, Ghannoum MA, Perfect JR (2006) Zygomycosis: the re-emerging fungal infection. Eur J Clin Microbiol Infect Dis 25:215–229PubMedCrossRefGoogle Scholar
  29. Csernetics Á, Nagy G, Iturriaga EA, Szekeres A, Eslava AP, Vágvölgyi CS, Papp T (2011) Expression of three isoprenoid biosynthesis genes and their effects on the carotenoid production of the zygomycete Mucor circinelloides. Fungal Genet Biol 48:696–703PubMedCrossRefGoogle Scholar
  30. Csernetics Á, Tóth E, Farkas A, Nagy G, Bencsik O, Vágvölgyi C, Papp T (2015) Expression of Xanthophyllomyces dendrorhous cytochrome-P450 hydroxylase and reductase in Mucor circinelloides. World J Microbiol Biotechnol 31:321–336PubMedCrossRefGoogle Scholar
  31. Czempinski K, Kruft V, Wöstemeyer J, Burmester A (1996) 4-dihydromethyltrisporate dehydrogenase from Mucor mucedo, an enzyme of the sexual hormone pathway:purification, and cloning of the corresponding gene. Microbiology 142:2647–2654PubMedCrossRefGoogle Scholar
  32. de Azevedo Santiago AL, de Souza Motta CM (2008) Isolation of Mucorales from processed maize (Zea mays L.) and screening for protease activity. Braz J Microbiol 39:698–700PubMedCentralPubMedCrossRefGoogle Scholar
  33. de Hoog GS, Guarro J, Genè J, Figueras MJ (2000) Zygomycota. In: Atlas of clinical fungi, pp 58–124, Centraalbureau voor Schimmelcultures, Universitat Rovira I Virgili, Utrecht, The NetherlandsGoogle Scholar
  34. de Hoog GS, Ibrahim AS, Voigt K (2014) Emerging zygomycetes: an emerging problem in the clinical laboratory. Mycoses 57(Suppl 3):1PubMedCentralPubMedCrossRefGoogle Scholar
  35. Dedyukhina E, Chistyakova T, Vainshtein M (2011) Biosynthesis of arachidonic acid by micromycetes (review). Appl Biochem Microbiol 47:109–117CrossRefGoogle Scholar
  36. Delalibera I Jr, Hajek AE, Humber RA (2003) Use of cell culture media for cultivation of the mite pathogenic fungi Neozygites tanajoae and Neozygites floridana. J Invertebr Pathol 84:119–127PubMedCrossRefGoogle Scholar
  37. Deng Y, Li S, Xu Q, Gao M, Huang H (2012) Production of fumaric acid by simultaneous saccharification and fermentation of starchy materials with 2-deoxyglucose-resistant mutant strains of Rhizopus oryzae. Bioresour Technol 107:363–367PubMedCrossRefGoogle Scholar
  38. Dolatabadi S, de Hoog GS, Meis JF, Walther G (2014a) Species boundaries and nomenclature of Rhizopus arrhizus (syn. R. oryzae). Mycoses 57:108–127PubMedCrossRefGoogle Scholar
  39. Dolatabadi S, Walther G, van den Ende AHGG, de Hoog GS (2014b) Diversity and delimitation of Rhizopus microsporus. Fungal Div 64:145–163CrossRefGoogle Scholar
  40. Dufossé L (2006) Microbial production of food grade pigments. Food Technol Biotechnol 44:313–321Google Scholar
  41. Dufossé L (2008) Pigments from microalgae and microorganisms: sources of food colorants. In: Sociaciu C (ed) Food colorants, chemical and functional properties. CRC Press, Boca Raton, FL, pp 399–427Google Scholar
  42. Dyal SD, Narine SS (2005) Implications for the use of Mortierella fungi in the industrial production of essential fatty acids. Food Res Int 38:445–467CrossRefGoogle Scholar
  43. Dyal SD, Bouzidi L, Narine SS (2005) Maximizing the production of γ-linolenic acid in Mortierella ramanniana var. ramanniana as a function of pH, temperature and carbon source, nitrogen source, metal ions and oil supplementation. Food Res Int 38:815–829CrossRefGoogle Scholar
  44. Fakas S, Papanikolaou S, Batsos A, Galiotou-Panayotou M, Mallouchos A, Aggelis G (2009) Evaluating renewable carbon sources as substrates for single cell oil production by Cunninghamella echinulata and Mortierella isabellina. Biomass Bioenergy 33:573–580CrossRefGoogle Scholar
  45. Ferreira JA, Lennartsson PR, Edebo L, Taherzadeh MJ (2013) Zygomycetes-based biorefinery: Present status and future prospects. Bioresour Technol 135:523–532PubMedCrossRefGoogle Scholar
  46. Fujimura R, Nishimura A, Ohshima S, Sato Y, Nishizawa T, Oshima K, Hattori M, Narisawa K, Ohta H (2014) Draft Genome Sequence of the Betaproteobacterial Endosymbiont Associated with the Fungus Mortierella elongata FMR23-6. Genome Announc 2(6):e01272-14PubMedCentralPubMedCrossRefGoogle Scholar
  47. Gao D, Zeng J, Zheng Y, Yu X, Chen S (2013) Microbial lipid production from xylose by Mortierella isabellina. Bioresour Technol 133:315–321PubMedCrossRefGoogle Scholar
  48. Garre V, Barredo JL, Iturriaga EA (2015) Transformation of Mucor circinelloides f. lusitanicus protoplasts. In: van den Berg MA, Maruthachalam K (eds) Genetic transformation systems in fungi, Volume 1. Springer International Publishing, pp 49–59Google Scholar
  49. Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G, Petiti L, Cruveiller S, Bianciotto V, Piffanelli P, Lanfranco L, Bonfante P (2012) The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. ISME J 6(1):136–145PubMedCentralPubMedCrossRefGoogle Scholar
  50. Goldberg I, Rokem JS, Pines O (2006) Organic acids: old metabolites, new themes. J Chem Tech Biotechnol 81:1601–1611CrossRefGoogle Scholar
  51. Gooday GW (1974) Fungal sex hormones. Annu Rev Biochem 43:35–49PubMedCrossRefGoogle Scholar
  52. Gopinath SCB, Anbu P, Lakshmipriya T, Hilda A (2013) Strategies to characterize fungal lipases for applications in medicine and dairy industry. Biomed Res Int 2013:1545–1549CrossRefGoogle Scholar
  53. Greenberg RN, Scott LJ, Vaughn HH, Ribes JA (2004) Zygomycosis (mucormycosis): emerging clinical importance and new treatments. Curr Opin Infect Dis 17:517–525PubMedCrossRefGoogle Scholar
  54. Grundschober A, Tuor U, Aebi M (1998) In vitro cultivation and sporulation of Neozygites parvispora (Zygomycetes: Entomophthorales). Syst Appl Microbiol 21:461–469CrossRefGoogle Scholar
  55. Gryganskyi AP, Lee SC, Litvintseva AP, Smith ME, Bonito G, Porter T, Anishchenko IM, Heitman J, Vilgalys R (2010) Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS One 5(12), e15273PubMedCentralPubMedCrossRefGoogle Scholar
  56. Guo Y, Yan Q, Jiang Z, Teng C, Wang X (2010) Efficient production of lactic acid from sucrose and corncob hydrolysate by a newly isolated Rhizopus oryzae GY18. J Ind Microbiol Biotechnol 37:1137–1143PubMedCrossRefGoogle Scholar
  57. Gutiérrez A, López-García S, Garre V (2011) High reliability transformation of the basal fungus Mucor circinelloides by electroporation. J Microbiol Met 84:442–446CrossRefGoogle Scholar
  58. Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. MycoKeys 1:7–20CrossRefGoogle Scholar
  59. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133PubMedCrossRefGoogle Scholar
  60. Hesseltine CW (1983) Microbiology of oriental fermented foods. Annu Rev Microbiol 37:575–601PubMedCrossRefGoogle Scholar
  61. Hesseltine CW (1991) Zygomycetes in food fermentations. Mycologist 5:162–169CrossRefGoogle Scholar
  62. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson O, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch T, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde K, Köljalb U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto R, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schuessler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang A, Weir A, Weiss M, White M, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547PubMedCrossRefGoogle Scholar
  63. Hoffmann K, Telle S, Walther G, Eckart M, Kirchmair M, Prillinger HJ, Prazenica A, Newcombe G, Dölz F, Papp T, Vágvölgyi C, de Hoog S, Olsson L, Voigt K (2009) Diversity, genotypic identification, ultrastructural and phylogenetic characterization of zygomycetes from different ecological habitats and climatic regions: limitations and utility of nuclear ribosomal DNA barcode markers. In: Gherbawy Y, Mach RL, Rai M (eds) Current advances in molecular mycology. Nova, New York, pp 263–312Google Scholar
  64. Hoffmann K, Voigt K, Kirk PM (2011) Mortierellomycotina subphyl. nov. based on multi-gene genealogies. Mycotaxon 115:353–363CrossRefGoogle Scholar
  65. Hoffmann K, Pawlowska J, Walther G, Wrzosek M, de Hoog GS, Benny GL, Kirk PM, Voigt K (2013) The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies. Persoonia 30:57–76PubMedCentralPubMedCrossRefGoogle Scholar
  66. Hou C (2008) Production of arachidonic acid and dihomo-linolenic acid from glycerol by oil-producing filamentous fungi, Mortierella in the ARS culture collection. J Ind Microbiol Biotechnol 35:501–506PubMedCrossRefGoogle Scholar
  67. Huang C, Chen XF, Xiong L, Chen XD, Ma LL, Chen Y (2013) Single cell oil production from low-cost substrates: the possibility and potential of its industrialization. Biotechnol Adv 31(2):129–139PubMedCrossRefGoogle Scholar
  68. Ibrahim AS (2011) Host cell invasion in mucormycosis: role of iron. Curr Opin Microbiol 14:406–411PubMedCentralPubMedCrossRefGoogle Scholar
  69. Ibrahim AS, Gebremariam T, Liu M, Chamilos G, Kontoyiannis DP, Mink R, Kwon-Chung KJ, Fu Y, Skory CD, Edwards JE Jr, Spellberg B (2008) Bacterial Endosymbiosis is widely present among Zygomycetes but does not contribute to the pathogenesis of mucormycosis. J Infect Dis 198:1083–1090PubMedCentralPubMedCrossRefGoogle Scholar
  70. Ikubo S, Takigawa N, Ueoka H, Kiura K, Tabata M, Shibayama T, Chikamori M, Aoe K, Matsushita A, Harada M (1999) In vitro evaluation of antimicrotubule agents in human small-cell lung cancer cell lines. Anticancer Res 19:3985–3988PubMedGoogle Scholar
  71. Iturriaga EA, Díaz-Mínguez JM, Benito EP, Álvarez MI, Eslava AP (1992) Heterologous transformation of Mucor circinelloides with the Phycomyces blakesleeanus leu1 gene. Curr Genet 21:215–223PubMedCrossRefGoogle Scholar
  72. Iturriaga EA, Velayos A, Eslava AP (2000) The structure and function of the genes involved in the biosynthesis of carotenoids in the Mucorales. Biotechnol Bioprocess Eng 5:263–274CrossRefGoogle Scholar
  73. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of the fungi using a six-gene phylogeny. Nature 443:818–822PubMedCrossRefGoogle Scholar
  74. Jang HD, Lin YY, Yang SS (2000) Polyunsaturated fatty acid production with Mortierella alpina by solid substrate fermentation. Bot Bull Acad Sin 41:41–48Google Scholar
  75. Jennessen J, Nielsen KF, Houbraken J, Lyhne EK, Schnürer J, Frisvad JC, Samson RA (2005) Secondary metabolite and mycotoxin production by the Rhizopus microsporus group. J Agric Food Chem 53(5):1833–1840PubMedCrossRefGoogle Scholar
  76. Jin B, Yin P, Ma Y, Zhao L (2005) Production of lactic acid and fungal biomass by Rhizopus fungi from food processing waste water. J Ind Microbiol Biotechnol 32:678–686PubMedCrossRefGoogle Scholar
  77. Jones SK Jr, Bennett RJ (2011) Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 48:668–676PubMedCentralPubMedCrossRefGoogle Scholar
  78. Karimi K, Zamani A (2013) Mucor indicus: biology and industrial application perspectives: a review. Biotechnol Adv 31:466–481PubMedCrossRefGoogle Scholar
  79. Kauffman CA (2004) Zygomycosis: reemergence of an old pathogen. Clin Infect Dis 39:588–590PubMedCrossRefGoogle Scholar
  80. Kavadia A, Komaitis M, Chevalot I, Blanchard F, Marc I, Aggelis G (2001) Lipid and gamma-linolenic acid accumulation in strains of zygomycetes growing on glucose. J Am Oil Chem Soc 78:341–346CrossRefGoogle Scholar
  81. Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 8:267–269CrossRefGoogle Scholar
  82. Krisch J, Takó M, Papp T, Vágvölyi C (2010) Characteristics and potential use of β-glucosidases from Zygomycetes. In: Méndez-Vilas a (ed.) Current research, technology and education topics in applied microbiology and microbial biotechnology, Formatex Research Center, pp 891-896.Google Scholar
  83. Krizsán K, Bencsik O, Nyilasi I, Galgóczy L, Vágvölgyi C, Papp T (2010) Effect of the sesterterpene-type metabolites, ophiobolins A and B, on zygomycetes fungi. FEMS Microbiol Lett 313:135–140PubMedCrossRefGoogle Scholar
  84. Lee S, Jang Y, Lee YM, Lee J, Lee H, Kim GH, Kim JJ (2011) Rice straw-decomposing fungi and their cellulolytic and xylanolytic enzymes. J Microbiol Biotechnol 21:1322–1329PubMedCrossRefGoogle Scholar
  85. Lee SC, Billmyre RB, Li A, Carson S, Sykes SM, Huh EY, Mieczkowski P, Ko DC, Cuomo CA, Heitman J (2014) Analysis of a food-borne fungal pathogen outbreak: virulence and genome of a Mucor circinelloides isolate from yogurt. mBio 5(4):e01390-14PubMedCentralPubMedCrossRefGoogle Scholar
  86. Lennartsson PR, Karimi K, Edebo L, Taherzadeh MJ (2009) Effects of different growth forms of Mucor indicus on cultivation on dilute-acid lignocellulosic hydrolyzate, inhibitor tolerance, and cell wall composition. J Biotechnol 143:255–261PubMedCrossRefGoogle Scholar
  87. Lichtwardt RW, Manier JF (1978) Validation of the Harpellales and Asellariales. Mycotaxon 7:441–442Google Scholar
  88. Liu XJ, Liu RS, Li HM, Tang YJ (2012) Lycopene production from synthetic medium by Blakeslea trispora NRRL2895(+) and 2896(-) in a stirred-tank fermenter. Bioprocess Biosyst Eng 35:739–749PubMedCrossRefGoogle Scholar
  89. Lukács GY, Papp T, Somogyvári F, Csernetics Á, Nyilasi I, Vágvölgyi CS (2009) Cloning of the Rhizomucor miehei 3-hydroxy-3-methylglutaryl-coenzyme A reductase gene and its heterologous expression in Mucor circinelloides. Ant Leeuwenhoek 95:55–64CrossRefGoogle Scholar
  90. Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, Abe A, Calvo SE, Corrochano LM, Engels R, Fu J, Hansberg W, Kim JM, Kodira CD, Koehrsen MJ, Liu B, Miranda-Saavedra D, O’Leary S, Ortiz-Castellanos L, Poulter R, Rodriguez-Romero J, Ruiz-Herrera J, Shen YQ, Zeng Q, Galagan J, Birren BW, Cuomo CA, Wickes BL (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5, e1000549PubMedCentralPubMedCrossRefGoogle Scholar
  91. Medina HR, Cerdá-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82(1):199–208PubMedCrossRefGoogle Scholar
  92. Mehta BJ, Salgado LM, Bejarano ER, Cerdá-Olmedo E (1997) New mutants of Phycomyces blakesleeanus for beta-carotene production. Appl Environ Microbiol 63:3657–3661PubMedCentralPubMedGoogle Scholar
  93. Mendoza L, Vilela R, Voelz K, Ibrahim AS, Voigt K, Lee SC (2014) Human fungal pathogens of Mucorales and Entomophthorales, Chapter 27. In: Casadevall A, Mitchell AP, Berman J, Kwon-Chung KJ, Perfect JR, Heitman J (eds) Cold spring harbor perspectives: fungal pathogens. Cold Spring Harbor Press, Cold Spring Harb Perspect Med 5(4) pii: a019562Google Scholar
  94. Meussen BJ, de Graaff LH, Sanders JP, Weusthuis RA (2012) Metabolic engineering of Rhizopus oryzae for the production of platform chemicals. Appl Microbiol Biotechnol 94:875–886PubMedCentralPubMedCrossRefGoogle Scholar
  95. Millati R, Edebo L, Taherzadeh MJ (2005) Performance of Rhizopus, Rhizomucor, and Mucor in ethanol production from glucose, xylose, and wood hydrolyzates. Enzyme Microb Technol 36:294–300CrossRefGoogle Scholar
  96. Monteiro de Souza P, de Oliveira Magalhães P (2010) Application of microbial α-amylase in industry – a review. Braz J Microbiol 41(4):850–861Google Scholar
  97. Morace G, Borghi E (2012) invasive mold infections: virulence and pathogenesis of mucorales. Int J Microbiol 2012, Article ID 349278, 5 pGoogle Scholar
  98. Moss ST (1975) Commensalism of the trichomycetes. In: Batra LR (ed) Insect-fungus symbiosis: nutrition, mutualism and commensalism. Allanheld, Osmun & Co., Montclair, pp 175–227Google Scholar
  99. Mullaney EJ, Ullah AH (2003) The term phytase comprises several different classes of enzymes. Biochem Biophys Res Commun 312:179–184PubMedCrossRefGoogle Scholar
  100. Mullaney EJ, Daly CB, Ullah AH (2000) Advances in phytase research. Adv Appl Microbiol 47:157–199PubMedCrossRefGoogle Scholar
  101. Münchberg U, Wagner L, Spielberg ET, Voigt K, Rösch P, Popp J (2012) Spatially resolved investigation of the oil composition in single intact hyphae of Mortierella spp. with micro-Raman spectroscopy. Biochim Biophys Acta 1831:341–349PubMedCrossRefGoogle Scholar
  102. Münchberg U, Wagner L, Rohrer C, Voigt K, Jahreis G, Rösch P, Popp J (2015) Quantitative assessment of the degree of lipid unsaturation in intact Mortierella by Raman microspectroscopy. Anal Bioanal Chem 407:3303–3311PubMedCrossRefGoogle Scholar
  103. Nagy LG, Petkovits T, Kovács GM, Voigt K, Vágvölgyi C, Papp T (2011) Where is the unseen fungal diversity hidden? A study of Mortierella reveals a large contribution of reference collections to the identification of fungal environmental sequences. New Phytol 191:789–794PubMedCrossRefGoogle Scholar
  104. Nagy G, Farkas A, Csernetics Á, Bencsik O, Szekeres A, Nyilasi I, Vágvölgyi CS, Papp T (2014) Transcription analysis of the three HMG-CoA reductase genes of Mucor circinelloides. BMC Microbiol 14:93PubMedCentralPubMedCrossRefGoogle Scholar
  105. Nahas E (1988) Control of lipase production by Rhizopus oligosporus under various growth conditions. J Gen Microbiol 134:227–233Google Scholar
  106. Navarro E, Lorca-Pascual JM, Quiles-Rosillo MD, Nicolas FE, Garre V, Torres-Martinez S, Ruiz-Vazquez RM (2001) A negative regulator of light-inducible carotenogenesis in Mucor circinelloides. Mol Gen Genomics 266:463–470CrossRefGoogle Scholar
  107. Navarro E, Peñaranda A, Hansberg W, Torres-Martínez S, Garre V (2013) A white collar 1-like protein mediates opposite regulatory functions in Mucor circinelloides. Fungal Genet Biol 52:42–52PubMedCrossRefGoogle Scholar
  108. Nicolás-Molina FE, Navarro E, Ruiz-Vázquez RM (2008) Lycopene over-accumulation by disruption of the negative regulator gene crgA in Mucor circinelloides. Appl Microbiol Biotechnol 78:131–137PubMedCrossRefGoogle Scholar
  109. Nout MJR, Kiers JL (2005) Tempeh fermentation, innovation and functionality: update into the third millennium. J Appl Microbiol 98:789–805PubMedCrossRefGoogle Scholar
  110. Nützmann HW, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, Gacek A, Schümann J, Hertweck C, Strauss J, Brakhage AA (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci USA 108(34):14282–14287PubMedCentralPubMedCrossRefGoogle Scholar
  111. Nützmann HW, Schroeckh V, Brakhage AA (2012) Regulatory cross talk and microbial induction of fungal secondary metabolite gene clusters. Methods Enzymol 517:325–341PubMedCrossRefGoogle Scholar
  112. Obraztsova IN, Prados N, Holzmann K, Avalos J, Cerda-Olmedo E (2004) Genetic damage following introduction of DNA in Phycomyces. Fungal Genet Biol 41:68–180CrossRefGoogle Scholar
  113. Orlowsky M (1991) Mucor dimorphism. Microbiol Rev 55:234–258Google Scholar
  114. Osmani SA, Scrutton MC (1985) The sub-cellular localisation and regulatory properties of pyruvate carboxylase from Rhizopus arrhizus. Eur J Biochem 147:119–128PubMedCrossRefGoogle Scholar
  115. Overman SA, Romano AH (1969) Pyruvate carboxylase of Rhizopus nigricans and its role in fumaric acid production. Biochem Biophys Res Commun 37:457–463PubMedCrossRefGoogle Scholar
  116. Papp T, Velayos A, Bartók T, Eslava AP, Vágvölgyi CS, Iturriaga EA (2006) Heterologous expression of astaxanthin biosynthesis genes in Mucor circinelloides. Appl Microbiol Biotechnol 69:526–531PubMedCrossRefGoogle Scholar
  117. Papp T, Csernetics Á, Nyilasi I, Ábrók M, Vágvölgyi CS (2010) Genetic transformation of Zygomycetes fungi. In: Rai MK, Kövics GJ (eds) Progress in mycology. Springer, Netherlands, pp 75–94CrossRefGoogle Scholar
  118. Papp T, Hoffmann K, Nyilasi I, Petkovits T, Wagner L, Vágvölgyi C, Voigt K (2011) Mortierella. In: Liu D (ed) Molecular detection of human fungal pathogens. Taylor & Francis CRC Press, pp 749–758Google Scholar
  119. Papp T, Csernetics Á, Nagy G, Bencsik O, Iturriaga EA, Eslava AP, Vágvölgyi CS (2013) Canthaxanthin production with modified Mucor circinelloides strains. Appl Microbiol Biotechnol 97:4937–4950PubMedCrossRefGoogle Scholar
  120. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 10:763–775CrossRefGoogle Scholar
  121. Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888PubMedCrossRefGoogle Scholar
  122. Partida-Martinez LP, Bandemer S, Rüchel R, Dannaoui E, Hertweck C (2008) Lack of evidence of endosymbiotic toxin-producing bacteria in clinical Rhizopus isolates. Mycoses 51(3):266–269PubMedCrossRefGoogle Scholar
  123. Petrič S, Hakki T, Bernhardt R, Zigon D, Crešnar B (2010) Discovery of a steroid 11α-hydroxylase from Rhizopus oryzae and its biotechnological application. J Biotechnol 150:428–437PubMedCrossRefGoogle Scholar
  124. Polaino S, Herrador MM, Cerdá-Olmedo E, Barrero AF (2010) Splitting of beta-carotene in the sexual interaction of Phycomyces. Org Biomol Chem 8(19):4229–4231PubMedCrossRefGoogle Scholar
  125. Poliakov E, Gentleman S, Cunningham FX Jr, Miller-Ihli NJ, Redmond TM (2005) Key role of conserved histidines in recombinant mouse beta-carotene 15´15-monooxygenase-1 activity. J Biol Chem 280:29217–29223PubMedCrossRefGoogle Scholar
  126. Pritchard GG (1971) An NAD + -independent L-lactate dehydrogenase from Rhizopus oryzae. Biochim Biophys Acta 250:25–34PubMedCrossRefGoogle Scholar
  127. Pritchard GG (1973) Factors affecting the activity and synthesis of NAD dependent lactate dehydrogenase in Rhizopus oryzae. J Gen Microbiol 78:125–137CrossRefGoogle Scholar
  128. Quiles-Rosillo MD, Ruiz-Vázquez RM, Torres-Martínez S, Garre V (2003) Cloning, characterization and heterologous expression of the Blakeslea trispora gene encoding orotidine-5P-monophosphate decarboxylase. FEMS Microbiol Lett 222:229–236PubMedCrossRefGoogle Scholar
  129. Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for Single Cell Oil production. Biochimie 86:807–815PubMedCrossRefGoogle Scholar
  130. Ratledge C, Wynn JP (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51PubMedCrossRefGoogle Scholar
  131. Revuelta JL, Eslava AP (1983) A new gene (carC) involved in the regulation of carotenogenesis in Phycomyces. Mol Gen Genet 192:225–229CrossRefGoogle Scholar
  132. Ribes JA, Vanover-Sams CL, Baker DJ (2000) Zygomycetes in human disease. Clin Microbiol Rev 13(2):236–301PubMedCentralPubMedCrossRefGoogle Scholar
  133. Roa Engel CA, Straathof AJ, Zijlmans TW, van Gulik WM, van der Wielen LA (2008) Fumaric acid production by fermentation. Appl Microbiol Biotechnol 78:379–389PubMedCentralPubMedCrossRefGoogle Scholar
  134. Rodríguez-Ortiz R, Michielse C, Rep M, Limón MC, Avalos J (2012) Genetic basis of carotenoid overproduction in Fusarium oxysporum. Fungal Genet Biol 49:684–696PubMedCrossRefGoogle Scholar
  135. Rodríguez-Sáiz M, Paz B, de la Fuente JL, López-Nieto MJ, Cabri W, Barredo JL (2004) Blakeslea trispora genes for carotene biosynthesis. Appl Environ Microbiol 70:5589–5594PubMedCentralPubMedCrossRefGoogle Scholar
  136. Rodríquez-Sáiz M, de la Fuente JL, Barredo JL (2012) Metabolic engineering of Mucor circinelloides for zeaxanthin production. Methods Mol Biol 898:133–151CrossRefGoogle Scholar
  137. Roncero MIG, Cerdá-Olmedo E (1982) Genetics of carotene biosynthesis in Phycomyces. Curr Genet 5:5–8PubMedCrossRefGoogle Scholar
  138. Rothhardt J, Schwartze V, Voigt K (2011) Entomophthorales. In: Liu D (ed) Molecular detection of human fungal pathogens. Taylor & Francis CRC Press, pp 723–734Google Scholar
  139. Ruiz-Hidalgo MJ, Benito EP, Sandmann G, Eslava AP (1997) The phytoene dehydrogenase gene of Phycomyces: regulation of its expression by blue light and vitamin A. Mol Gen Genet 253:734–744PubMedCrossRefGoogle Scholar
  140. Ruiz-Hidalgo MJ, Eslava AP, Alvarez MI, Benito EP (1999) Heterologous expression of the Phycomyces blakesleeanus phytoene dehydrogenase gene (carB) in Mucor circinelloides. Curr Microbiol 39:259–264PubMedCrossRefGoogle Scholar
  141. Sahadevan Y, Richter-Fecken M, Kaerger K, Voigt K, Boland W (2013) Early and late trisporoids differentially regulate β-carotene production and gene transcript Levels in the mucoralean fungi Blakeslea trispora and Mucor mucedo. Appl Environ Microbiol 79(23):7466–7475PubMedCentralPubMedCrossRefGoogle Scholar
  142. Saito K, Saito A, Ohnishi M, Oda Y (2004) Genetic diversity in Rhizopus oryzae strains as revealed by the sequence of lactate dehydrogenase genes. Arch Microbiol 182:30–36PubMedCrossRefGoogle Scholar
  143. Sajbidor J, Certik M, Dobronova S (1988) Influence of different carbon sources on growth, lipid content and fatty acid composition in four strains belonging to Mucorales. Biotechnol Lett 10:347–350CrossRefGoogle Scholar
  144. Salgado LM, Bejarano ER, Cerdá-Olmedo E (1989) Carotene superproducing mutants of Phycomyces blakesleeanus. Exp Mycol 13:332–336CrossRefGoogle Scholar
  145. Sanz C, Velayos A, Álvarez MI, Benito EP, Eslava AP (2011) Functional analysis of the Phycomyces carRA gene encoding the enzymes phytoene synthase and lycopene cyclase. PLos One 6:e23102PubMedCentralPubMedCrossRefGoogle Scholar
  146. Sato Y, Narisawa K, Tsuruta K, Umezu M, Nishizawa T, Tanaka K, Yamaguchi K, Komatsuzaki M, Ohta H (2010) Detection of Betaproteobacteria inside the mycelium of the fungus Mortierella elongata. Microbes Environ 25(4):321–324PubMedCrossRefGoogle Scholar
  147. Sautour M, Soares Mansur C, Divies C, Bensoussan M, Dantigny P (2002) Comparison of the effects of temperature and water activity on growth rate of food spoilage moulds. J Ind Microbiol Biotechnol 28:311–315PubMedCrossRefGoogle Scholar
  148. Scarborough CL, Ferrari J, Godfray HC (2005) Aphid protected from pathogen by endosymbiont. Science 310(5755):1781PubMedCrossRefGoogle Scholar
  149. Schachtschabel D, Schimek C, Wöstemeyer J, Boland W (2005) Biological activity of trisporoids and trisporoid analogues in Mucor mucedo (-). Phytochemistry 66(11):1358–1365PubMedCrossRefGoogle Scholar
  150. Schachtschabel D, David A, Menzel KD, Schimek C, Wöstemeyer J, Boland W (2008) Cooperative biosynthesis of trisporoids by the (+) and (-) mating types of the zygomycete Blakeslea trispora. ChemBioChem 9(18):3004–3012PubMedCrossRefGoogle Scholar
  151. Schimek C, Wöstemeyer J (2009) Carotene derivatives in sexual communication of zygomycete fungi. Phytochemistry 70:1867–1875PubMedCrossRefGoogle Scholar
  152. Schimek C, Kleppe K, Saleem AR, Voigt K, Burmester A, Wöstemeyer J (2003) Sexual reactions in Mortierellales are mediated by the trisporic acid system. Mycol Res 107:736–747PubMedCrossRefGoogle Scholar
  153. Schroeckh V, Scherlach K, Nützmann HW, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA 106(34):14558–14563PubMedCentralPubMedCrossRefGoogle Scholar
  154. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872PubMedCrossRefGoogle Scholar
  155. Schwartze VU, Winter S, Shelest E, Marcet-Houben M, Horn F, Wehner S, Linde J, Valiante V, Sammeth M, Riege K, Nowrousian M, Kaerger K, Jacobsen ID, Marz M, Brakhage AA, Gabaldón T, Böcker S, Voigt K (2014) Gene expansion shapes genome architecture in the human pathogen Lichtheimia corymbifera: an evolutionary genomics analysis in the ancient terrestrial Mucorales (Mucoromycotina). PLoS Genet 10(8):e1004496. doi: 10.1371/journal.pgen.1004496 PubMedCentralPubMedCrossRefGoogle Scholar
  156. Serrano I, Lopes da Silva T, Carlos Roseiro J (2001) Ethanol-induced dimorphism and lipid composition changes in Mucor fragilis CCMI 142. Lett Appl Microbiol 33:89–93PubMedCrossRefGoogle Scholar
  157. Sharifia M, Karimi K, Taherzadeh MJ (2008) Production of ethanol by filamentous and yeast-like forms of Mucor indicus from fructose, glucose, sucrose, and molasses. J Ind Microbiol Biotechnol 35:1253–1259PubMedCrossRefGoogle Scholar
  158. Shelest E (2008) Transcription factors in fungi. FEMS Microbiol Lett 286:145–151PubMedCrossRefGoogle Scholar
  159. Shelest E, Voigt K (2014) Genomics to study basal lineage fungal biology: phylogenomics suggests a common origin. In: Nowrousian M (ed) The Mycota, vol XIII, 2nd edn, Fungal genomics. Springer, Berlin, pp 31–60Google Scholar
  160. Sigel R, Sigel A, Sigel H (2007) The ubiquitous roles of cytochrome P450 proteins: metal ions in life sciences. Wiley, New York. ISBN 0-470-01672-8CrossRefGoogle Scholar
  161. Silva F, Torres-Martinez S, Garre V (2006) Distinct white collar-1 genes control specific light responses in Mucor circinelloides. Mol Microbiol 61:1023–1037PubMedCrossRefGoogle Scholar
  162. Silva F, Navarro E, Peñaranda A, Murcia-Flores L, Torres-Martínez S, Garre V (2008) A RING-finger protein regulates carotenogenesis via proteolysis-independent ubiquitylation of a white collar-1-like activator. Mol Microbiol 70:1026–1036PubMedGoogle Scholar
  163. Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and co-incidence with vascular land plants. Nature 363:67–69CrossRefGoogle Scholar
  164. Skory CD (2000) Isolation and expression of lactate dehydrogenase genes from Rhizopus oryzae. Appl Environ Microbiol 66:2343–2348PubMedCentralPubMedCrossRefGoogle Scholar
  165. Spano LA, Medeiros J, Mandels M (1976) Enzymatic hydrolysis of cellulose wastes to glucose. Resour Recover Conserv 1:279–294CrossRefGoogle Scholar
  166. Stredansky M, Conti E, Stredanska S, Zanetti F (2000) γ-Linolenic acid production with Thamnidium elegans by solid-state fermentation on apple pomace. Bioresour Technol 73:41–45CrossRefGoogle Scholar
  167. Sun J, Sun XX, Tang PW, Yuan QP (2012) Molecular cloning and functional expression of two key carotene synthetic genes derived from Blakeslea trispora into E. coli for increased β-carotene production. Biotechnol Lett 34:2077–2082PubMedCrossRefGoogle Scholar
  168. Tagua VG, Medina HR, Martín-Domínguez R, Eslava AP, Corrochano LM, Cerdá-Olmedo E, Idnurm A (2012) A gene for carotene cleavage required for pheromone biosynthesis and carotene regulation in the fungus Phycomyces blakesleeanus. Fungal Genet Biol 49(5):398–404PubMedCrossRefGoogle Scholar
  169. Takahashi Y, Moiseyev G, Chen Y, Ma JX (2005) Identification of conserved histidines and glutamic acid as key residues for isomerohydrolase activity of RPE65, an enzyme of the visual cycle in the retinal pigment epithelium. FEBS Lett 579:5414–5418PubMedCrossRefGoogle Scholar
  170. Torres-Martínez S, Murillo FJ, Cerdá-Olmedo E (1980) Genetics of locopene cyclization and substrate transfer in beta-carotene biosynthesis in Phycomyces. Genet Res 36:299–946PubMedCrossRefGoogle Scholar
  171. Tsuruo T, Oh-hara T, Iida H, Tsukagoshi S, Sato Z, Matsuda I, Iwasaki S, Okuda S, Shimizu F, Sasagawa K, Fukami M, Fukada K, Arakawa M (1986) Rhizoxin, a macrocyclic lactone antibiotic, as a new antitumor agent against human and murine tumor cells and their vincristine-resistant sublines. Cancer Res 46:381–385PubMedGoogle Scholar
  172. van der Westhuizen JPJ, Kock JLF, Botha A, Botes PJ (1994) The distribution of the ω3- and ω 6-series of cellular long-chain fatty acids in fungi. Sys Appl Microbiol 17:327–345CrossRefGoogle Scholar
  173. van Heeswijck R, Roncero MIG (1984) High frequency transformation of Mucor with recombinant plasmid DNA. Carlsberg Res Commun 49:691–702CrossRefGoogle Scholar
  174. Velayos A, Blasco JL, Alvarez MI, Iturriaga EA, Eslava AP (2000a) Blue-light regulation of the phytoene dehydrogenase (carB) gene expression in Mucor circinelloides. Planta 210:938–946PubMedCrossRefGoogle Scholar
  175. Velayos A, Eslava AP, Iturriaga EA (2000b) A bifunctional enzyme with lycopene cyclase and phytoene synthase activities is encoded by the carRP gene of Mucor circinelloides. Eur J Biochem 267:1–12CrossRefGoogle Scholar
  176. Velayos A, Papp T, Aguilar-Elena R, Fuentes-Vicente M, Eslava AP, Iturriaga EA, Álvarez MI (2003) Expression of the carG gene, encoding geranylgeranyl pyrophosphate synthase, is up-regulated by blue light in Mucor circinelloides. Curr Genet 43:112–120PubMedGoogle Scholar
  177. Velayos A, Fuentes-Vicente M, Aguilar-Elena R, Eslava AP, Iturriaga EA (2004) A novel fungal prenyl diphosphate synthase in the dimorphic zygomycete Mucor circinelloides. Curr Genet 45:371–377PubMedCrossRefGoogle Scholar
  178. Vially G, Marchal R, Guilbert N (2010) L(+) Lactate production from carbohydrates and lignocellulosic materials by Rhizopus oryzae UMIP 4.77. World J Microb Biot 26:607–614CrossRefGoogle Scholar
  179. Voigt K (2012) Zygomycota. In: Frey W (ed) Syllabus of plant families – A. Engler’s Syllabus der Pflanzenfamilien. Part 1/1: Blue-green algae, Myxomycetes and Myxomycete-like organisms, Phytoparasitic protists, Heterotrophic Heterokontobionta and Fungi p.p. Borntraeger Verlag, Stuttgart, pp 130–162Google Scholar
  180. Voigt K, de Hoog GS (2013) The zygomycetes in a phylogenetic perspective. Special issue Persoonia: molecular phylogeny and evolution of fungi, vol. 30. Naturalis Biodiversity Center Leiden and Centraalbureau voor Schimmelcultures Utrecht, The Netherlands, p 125Google Scholar
  181. Voigt K, Kirk PM (2014) 136. FUNGI | Classification of the zygomycetes: reappraisal as coherent class based on a comparison between traditional versus molecular systematics. In: Batt CA, Tortorello ML (eds) Encyclopedia of food microbiology, Vol 2. Elsevier, Academic, pp 54–67Google Scholar
  182. Voigt K, Wöstemeyer J (2001) Phylogeny and origin of 82 zygomycetes from all 54 genera of the Mucorales and Mortierellales based on combined analysis of actin and translation elongation factor EF-1α genes. Gene 270:113–120PubMedCrossRefGoogle Scholar
  183. Voigt K, Hoffmann K, Einax E, Eckart M, Papp T, Vágvölgyi C, Olsson L (2009) Revision of the family structure of the Mucorales (Mucoromycotina, Zygomycetes) based on multigene-genealogies: phylogenetic analyses suggest a bigeneric Phycomycetaceae with Spinellus as sister group to Phycomyces. In: Gherbawy Y, Mach RL, Rai M (eds) Current advances in molecular mycology. Nova, New York, pp 313–332Google Scholar
  184. Voigt K, Marano AV, Gleason F (2013) Ecological and economical importance of parasitic and zoosporic true fungi. In: Kempken F (ed) The Mycota, vol XI, 2nd edn, Agricultural applications. Springer, Berlin, pp 243–270Google Scholar
  185. Wagner L, Stielow B, Hoffmann K, Petkovits T, Papp T, Vágvölgyi C, de Hoog GS, Verkley G, Voigt K (2013) A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA. Persoonia 30:77–93PubMedCentralPubMedCrossRefGoogle Scholar
  186. Wang GY, Keasling JD (2002) Amplification of HMG-CoA reductase production enhances carotenoid accumulation in Neurospora crassa. Metab Eng 4:193–201PubMedCrossRefGoogle Scholar
  187. Wang L, Chen W, Feng Y, Ren Y, Gu Z et al (2011) Genome characterization of the oleaginous fungus Mortierella alpina. PLoS One 6:e28319PubMedCentralPubMedCrossRefGoogle Scholar
  188. Wang D, Wu R, Xu Y, Li M (2013) Draft genome sequence of Rhizopus chinensis CCTCCM201021, used for brewing traditional Chinese alcoholic beverages. Genome Announc 1(2), e0019512PubMedGoogle Scholar
  189. Werpy T, Petersen G (2004) Top value added chemicals from biomass, vol 1, Results of screening for potential candidates from sugars and synthesis gas. US Department of Energy, Washington, DCGoogle Scholar
  190. Wetzel J, Scheibner O, Burmester A, Schimek C, Wöstemeyer J (2009) 4-Dihydrotrisporin-dehydrogenase, an enzyme of the sex hormone pathway of Mucor mucedo: purification, cloning of the corresponding gene, and developmental expression. Eukaryotic Cell 8:88–95PubMedCentralPubMedCrossRefGoogle Scholar
  191. White JD, Blakemore PR, Green NJ et al (2002) Total synthesis of rhizoxin D, a potent antimitotic agent from the fungus Rhizopus chinensis. J Org Chem 67:7750–7760PubMedCrossRefGoogle Scholar
  192. Whittaker RH (1969) New concepts of kingdoms of organisms. Science 163:150–160PubMedCrossRefGoogle Scholar
  193. Wikandari R, Millati R, Lennartsson PR, Harmayani E, Taherzadeh MJ (2012) Isolation and characterization of zygomycetes fungi from tempeh for ethanol production and biomass applications. Appl Biochem Biotechnol 167:1501–1512PubMedCrossRefGoogle Scholar
  194. Willke T, Vorlop KD (2004) Industrial bioconversion of renewable resources as an alternative to conventional chemistry. Appl Microbiol Biotechnol 66:131–142PubMedCrossRefGoogle Scholar
  195. Wolff AM, Arnau J (2002) Cloning of glyceraldehyde-3-phosphate dehydrogenase-encoding genes in Mucor circinelloides (Syn. racemosus) and use of the gpd1 promoter for recombinant protein production. Fungal Genet Biol 35:21–29PubMedCrossRefGoogle Scholar
  196. Wöstemeyer J, Burmester A, Wöstemeyer A, Schultze K, Voigt K (2002) Gene transfer in the fungal host-parasite system Absidia glauca-Parasitella parasitica depends on infection. In: Syvanen M, Kado CI (eds) Horizontal gene transfer, 2nd edn. Academic, San Diego, CA, pp 241–247, Chapter 21CrossRefGoogle Scholar
  197. Wöstemeyer J, Grünler A, Schimek C, Voigt K (2005) Genetic regulation of carotenoid biosynthesis in fungi. In: Applied mycology and biotechnology Vol 5: Genes and genomics. Elsevier, pp 257–274Google Scholar
  198. Yen HW, Lee YC (2010) Production of lactic acid from raw sweet potato powders by rhizopus oryzae immobilized in sodium alginate capsules. Appl Biochem Biotechnol 162:607–615PubMedCrossRefGoogle Scholar
  199. Zeng J, Zheng Y, Yu X, Yu L, Gao D, Chen S (2013) Lignocellulosic biomass as a carbohydrate source for lipid production by Mortierella isabellina. Bioresour Technol 128:385–391PubMedCrossRefGoogle Scholar
  200. Zhang ZY, Jin B, Kelly JM (2007) Production of lactic acid from renewable materials by Rhizopus fungi. Biochem Eng J 35:251–263CrossRefGoogle Scholar
  201. Zorn H, Langhoff S, Scheibner M, Berger RG (2003) Cleavage of β-carotene to flavor compounds by fungi. Appl Microbiol Biotechnol 62(4):331–336PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Kerstin Voigt
    • 1
    • 2
  • Thomas Wolf
    • 3
  • Katrin Ochsenreiter
    • 4
  • Gábor Nagy
    • 5
  • Kerstin Kaerger
    • 6
  • Ekaterina Shelest
    • 3
  • Tamás Papp
    • 5
  1. 1.Jena Microbial Resource Collection, Leibniz Institute for Natural Product Research and Infection Biology – Hans-Knöll-InstituteJenaGermany
  2. 2.Department of Microbiology and Molecular Biology, Institute of MicrobiologyUniversity of JenaJenaGermany
  3. 3.Systems Biology/Bioinformatics, Leibniz Institute for Natural Product Research and Infection Biology – Hans-Knöll-InstituteJenaGermany
  4. 4.Karlsruhe Institute of Technology (KIT), Institute of Process Engineering in Life Sciences, Section II: Technical BiologyKarlsruheGermany
  5. 5.Faculty of Science and Informatics, Department of MicrobiologyUniversity of SzegedSzegedHungary
  6. 6.National Reference Center for Invasive Mycoses, Leibniz Institute for Natural Product Research and Infection Biology – Hans-Knöll-InstituteJenaGermany

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